Download as pdf or txt
Download as pdf or txt
You are on page 1of 12

AJN Patient-Oriented, Translational Research: Research Article

American Journal
of Nephrology Am J Nephrol Received: May 8, 2023
Accepted: July 13, 2023
DOI: 10.1159/000532109 Published online: August 3, 2023

Effects of Different Exercises on Physical


Function, Dialysis Adequacy, and
Health-Related Quality of Life in Maintenance
Hemodialysis Patients: A Systematic Review and

Downloaded from http://karger.com/ajn/article-pdf/doi/10.1159/000532109/3998785/000532109.pdf by guest on 20 November 2023


Network Meta-Analysis
Huagang Hu a, b Chanchan Wu a Jojo Yan Yan Kwok a Mu-Hsing Ho a
Pui Hing Chau a Kris Yuet Wan Lok a Edmond Pui Hang Choi a
aSchool of Nursing, LKS Faculty of Medicine, The University of Hong Kong, Hong Kong, China; bSchool of

Nursing, Suzhou Medical College of Soochow University, Suzhou, China

Keywords trials), dialysis adequacy (30 trials), and HRQOL (23 trials).
Exercise · Maintenance hemodialysis · Network meta-analysis Network meta-analysis showed that the most effective in-
tervention for walking capacity was intradialytic aerobic
exercise combined with blood flow restriction with a
Abstract mean difference and 95% confidence interval of 97.35
Background: Clinical guidelines recommend exercise (11.89–182.81), for peak oxygen uptake it was non-
training for patients undergoing maintenance hemodialysis intradialytic combined aerobic and resistance exercise
(MHD). However, the effectiveness of different types of with a value of 4.35 (2.25–6.44), for dialysis adequacy it was
exercise remains uncertain. Objectives: The aims of the intradialytic combined aerobic and resistance exercise with
study were to compare and rank the effect of different types a value of 0.17 (0.06–0.28), for the physical component
of exercise on walking capacity, cardiorespiratory fitness, summary of HRQOL it was intradialytic aerobic exercise with
dialysis adequacy, and health-related quality of life (HRQOL) a value of 4.93 (2.31–7.54), and for the mental component
in patients undergoing MHD. Methods: Eight databases summary of HRQOL it was non-intradialytic combined
(four English and four Chinese) were searched from in- aerobic and resistance exercise with a value of 6.36
ception to January 1, 2022. Randomized controlled trials (0.45–12.27). Ultimately, intradialytic combined aerobic and
evaluating the efficacy of different exercises for patients resistance exercise could improve all the above outcomes
undergoing MHD were included. Two independent re- compared to usual care. Conclusions: This study concluded
viewers screened the literature, extracted data, assessed the that intradialytic combined aerobic and resistance exercise
risk of bias, and evaluated the certainty of evidence. A is optimal for MHD patients due to its significant positive
frequentist random-effect network meta-analysis was con- effects on multiple outcomes. Walking capacity can be
ducted. Results: Ninety trials with 4,084 participants com-
paring 15 types of exercise were included, reporting on the Huagang Hu and Chanchan Wu contributed equally to this work and
six-minute walking test (45 trials), peak oxygen uptake (22 share first authorship.

karger@karger.com © 2023 The Author(s). Correspondence to:


www.karger.com/ajn Published by S. Karger AG, Basel Edmond Pui Hang Choi, h0714919 @ connect.hku.hk

This article is licensed under the Creative Commons Attribution-


NonCommercial 4.0 International License (CC BY-NC) (http://www.
karger.com/Services/OpenAccessLicense). Usage and distribution for
commercial purposes requires written permission.
further enhanced by combining blood flow restriction with sistance exercise (CE), and other types of exercise, they
exercise. For improving dialysis adequacy, intradialytic ex- grouped intradialytic and non-intradialytic exercises to-
ercise proves to be more effective than non-intradialytic gether, leaving it unclear which and when exercise is more
exercise. Further well-designed clinical trials are needed to effective for this population [12, 21, 22]. Different exercise
investigate the effects of exercise with varying durations, types have varying benefits for various outcomes. Exercises
intensities, and frequencies. © 2023 The Author(s). conducted during and out of hemodialysis may have unique
Published by S. Karger AG, Basel benefits and limitations [23]. Therefore, it is important to
evaluate the effect of different exercise types with a more
detailed classification, as this can provide direct evidence for
Introduction selecting exercise in clinical practice. The current NMA
aimed to synthesize the direct and indirect evidence to
The number of patients undergoing maintenance he- compare the effectiveness of different types of exercise for
modialysis (MHD) is continuously increasing worldwide walking capacity, cardiorespiratory fitness, dialysis ade-

Downloaded from http://karger.com/ajn/article-pdf/doi/10.1159/000532109/3998785/000532109.pdf by guest on 20 November 2023


[1]. Symptom clusters of renal disease, long dialysis duration, quacy, and HRQOL in MHD patients.
and multi-comorbidity contribute to inferior physical fitness
and poor health-related quality of life (HRQOL) in patients
undergoing MHD [2]. Cardiorespiratory fitness and walking Methods
capacity are important physical fitness indicators of great
concern to people with MHD, but their performance is Study Design
usually worse compared to their age-matched healthy This systematic review and NMA was conducted following the
counterparts [3, 4]. Impaired physical function and HRQOL Cochrane Handbook for Systematic Reviews of Interventions [24]
and reported according to the Preferred Reporting Items for Sys-
are associated with adverse outcomes, such as higher tematic Reviews and Meta-Analyses for Network Meta-Analysis
mortality and hospitalization rates [5]. (PRISMA-NMA) [20]. The protocol of this study was registered
Exercise training is an ideal alternative intervention for on the PROSPERO platform (reference: CRD42021286114).
MHD patients. According to the Renal Association Clinical
Practice Guideline on Hemodialysis, dialysis patients need Search Strategy and Selection Criteria
to do exercises, especially intradialytic exercises [6, 7]. Four English databases (PubMed, EMBASE, Cochrane Library,
and Web of Science) and four Chinese databases (WAN FANG
Traditional exercise types include aerobic, resistance, and Data; China National Knowledge Infrastructure; VIP Chinese
balance exercise [7]. Furthermore, recent years have seen Science and Technology Journal Database; Chinese BioMedical
the introduction of new elements in exercise protocols, such Literature Database) were searched from their inception to January
as virtual reality (VR) and blood flow restriction (BFR), 1, 2022. Two researchers (H.H. and W.C.) developed the search
which have been reported to be more effective than a single strategy and finalized it after consulting a senior researcher (EC).
The search strategy for PubMed is shown in online supplementary
type of exercise for MHD patients [7]. Several published Table 1 (for all online suppl. material, see https://doi.org/10.1159/
meta-analyses have shown that some exercise types could 000532109). The references of published systematic reviews were
improve walking capacity, cardiorespiratory fitness, dialysis also screened and searched for additional studies [4, 10–13, 17, 18,
adequacy, and HRQOL for MHD patients [8–18]. However, 25–28]. After deduplication, two reviewers (H.H. and W.C.) in-
the most effective exercise type for this population remains dependently screened titles, abstracts, and full-text of potentially
eligible studies based on the inclusion and exclusion criteria. Any
unknown [12, 19].
disagreements arising during the article selection process were
Pairwise meta-analysis could pool the impact of the same resolved after discussions among H.H., W.C., and E.C.
type of exercise compared to the usual care (UC), but it We conducted a comprehensive analysis of randomized controlled
could not conduct an indirect comparison between different trials published in English and Chinese to assess the effects of exercise
types of exercises [20]. In contrast, network meta-analysis on patients undergoing MHD. The study included adult participants
(NMA) can fill these gaps by synthesizing direct and in- (≥18 years old) who had been receiving hemodialysis treatment for at
least 3 months. All types of non-intradialytic and intradialytic exercise
direct comparisons to evaluate various intervention forms interventions were considered, with comparison groups comprising
and determine which is the most effective [20]. To date, UC and sham exercise. Exclusion criteria for this study were as
three NMA have been conducted to compare the effects of follows: participants receiving renal replacement therapies other than
different exercise types or intensities on cardiorespiratory hemodialysis (e.g., peritoneal dialysis or renal transplant); interven-
fitness, walking capacity, dialysis adequacy, and blood tions consisting solely of exercise instructions and education, rather
than specific exercise programs; single-session exercise interventions;
pressure in MHD patients [12, 21, 22]. Although these articles with abstracts only; studies with no relevant outcomes; and
published NMA compared the effect of UC, aerobic exercise studies lacking essential data after three attempts to contact authors
(AE), resistance exercise (RE), combined aerobic and re- via email.

2 Am J Nephrol Hu/Wu/Kwok/Ho/Chau/Lok/Choi
DOI: 10.1159/000532109
According to the literature review [3], the outcomes selected were • Step 5: using Egger test and visually inspected asymmetry of the
considered clinically important and of great concern to patients. The NMA funnel plots to assess the publication bias [35].
primary outcome of this study was walking capacity (assessed by the The statistical significance level is 0.05.
six-minute walking test, 6MWT). The secondary outcomes included
cardiorespiratory fitness (assessed by peak oxygen uptake, VO2peak),
dialysis adequacy (assessed by Kt/V, where K means dialyzer clear-
ance of urea, t means dialysis time, and V means the volume of Results
distribution of urea), and HRQOL. The HRQOL was assessed by the
Medical Outcomes Study Short-Form 36 (SF-36), 12-Item Short Study Characteristics
Form Survey (SF-12), or Kidney Disease and Quality of Life™ Short
Form which was included in SF-36 or SF-12. All of the above HRQOL We identified 6,832 records of potentially relevant
measurements have a standard score from 0 to 100, with higher scores publications, of which 253 articles were screened for full text
indicating better HRQOL [29]. (as shown in Fig. 1). Finally, 90 randomized controlled trials
involving 4,084 participants were included in this study (as
Data Extraction and Risk-Of-Bias Assessment shown in online suppl. Table S2), of which 85 studies were
published in English and five were published in Chinese.

Downloaded from http://karger.com/ajn/article-pdf/doi/10.1159/000532109/3998785/000532109.pdf by guest on 20 November 2023


Two independent researchers (H.H. and W.C.) carried out data
extraction and risk of bias assessment for the included studies
The sample size ranged from 13 to 234 participants. The
independently. Any disagreements were resolved through dis-
cussions with the senior researcher (E.C.). We developed and frequency of exercise ranged from 2 to 7 days per week, with
tested a data extraction form to gather basic article information the majority being 3 days (70/90 studies).
(title, setting, journal, publication year, language, etc.) and study The exercise types primarily consisted of AE (33 arms
details (number of participants, sociodemographic, duration of during dialysis and 9 arms outside of dialysis), RE (19
MHD, time and duration of implementation, types of intervention arms during dialysis and 2 arms outside of dialysis), and
and control, attrition, and outcomes). All relevant results from the
included studies were collected and analyzed. CE (22 arms during dialysis and 10 arms outside of
Two independent researchers conducted a risk of bias assessment dialysis). Most AE protocols involved cycling during
at the outcome level, utilizing the Risk of Bias tool 2.0 (RoB 2.0) from dialysis and walking or cycling outside of dialysis. REs
the Cochrane Collaboration [30]. The quality of evidence was eval- mainly focused on leg or nonvascular access side limb
uated using the Grading of Recommendations Assessment, Devel- exercises with ankle weights, dumbbells, elastic resistance
opment, and Evaluation (GRADE) for pairwise meta-analysis, as well
as the ranking of NMA [31]. The confidence in the NMA effect bands, or weight training machines during or outside of
estimates for all outcomes was assessed using the Confidence In dialysis. Other elements reported in exercise interven-
Network Meta-Analysis (CINeMA) approach [32]. tions for MHD patients included VR, BFR, functional
training, balance exercise, inspiratory muscle training
Statistical Analyses (IMT), and neuromuscular electrical stimulation, among
The mean difference (MD) and 95% confidence interval of others. The comparators consisted of UC (69 arms) and
changes from baseline to the end of intervention were used as the sham exercise (12 arms). Details of the interventions, the
effect estimate [24]. If the authors did not report the value of these
changes, we calculated them using the data from the baseline and control group, and their descriptions are presented in
end-of-study, as recommended by the Cochrane Handbook [24]. Table 1. The network plots for outcomes are shown in
First, we conducted a pairwise meta-analysis using a random-effect Figure 2. The size of the nodes represents the number of
analysis model with RevMan (Version 5.3, Cochrane) to make participants involved in each type of intervention, while
direct comparisons between interventions and comparators [33]. the thickness of lines between interventions indicates the
The χ2 test and I2 statistics were used to test the data heterogeneity
[34]. Second, a frequentist NMA was conducted via the mvmeta
number of studies comparing those interventions.
command in Stata (Version 14.1, Stata Corp., College Station, TX,
USA), following a five-step process [35]. Synthesis of Results
• Step 1: generating network geometry to explore the relation- Forty-five studies, featuring 98 arms and 15 types of
ships among interventions. interventions, reported on the 6MWT. The pairwise meta-
• Step 2: using the Wald χ2 test to assess global inconsistency and
analysis results revealed that, compared to UC, four types of
side-splitting to assess local inconsistency. If there was no
evidence of inconsistency, the consistency model was applied to intradialytic exercise (i.e., aerobic, resistance, combined
conduct the NMA with the random-effect model. aerobic and resistance, and IMT) significantly improved the
• Step 3: creating a league table to display the effect size by 6MWT with very low to low-quality evidence (as shown in
interventions. online suppl. Table S3). The NMA results indicated that nine
• Step 4: using the surface under the cumulative ranking (SU- exercise types could improve walking distance in MHD
CRA) and the probability of being best to identify the supe-
riority of interventions. When there are inconsistencies between patients compared with UC. The SUCRA ranking indicated
SUCRA and the probability of being best, SUCRA is considered that intradialytic AE (IAE) combined with BFR, intradialytic
the more reliable recommended estimate [35, 36]. IMT, and intradialytic RE (IRE) plus virtual reality were the

Exercise in Hemodialysis Patients Am J Nephrol 3


DOI: 10.1159/000532109
Downloaded from http://karger.com/ajn/article-pdf/doi/10.1159/000532109/3998785/000532109.pdf by guest on 20 November 2023
Fig. 1. PRISMA flow diagram of search process for studies examining the efficacy of exercise in MHD patients.

top three exercise modalities for improving the 6MWT. and 3.86 (2.24–5.49), respectively (as shown in Table 2,
These were followed by non-intradialytic CE (NCE) plus online suppl. Table S6; online suppl. Fig. S2). The con-
balance training, intradialytic CE (ICE), and IAE. Their effect fidence of the evidence for interventions was low for
sizes (MD, 95% confidence interval) paired with UC were VO2peak (as shown in Table 3; online suppl. Table S7).
97.35 (11.89–182.81), 77.27 (38.14–116.40), 77.98 A total of 30 studies with 66 arms and 11 types of in-
(5.85–150.12), 66.12 (7.88–124.35), 53.71 (30.08–77.35), and terventions were included in the analyses of Kt/V. The
51.14 (28.21–74.08), respectively (as shown in Table 2; online pairwise meta-analysis results showed that, compared to
suppl. Table S4; online suppl. Fig. S1). The confidence of the UC, IAE and intradialytic combined aerobic and resistance
evidence for interventions was moderate for the 6MWT (as could significantly improve the Kt/V with low quality of the
shown in Table 3; online suppl. Table S5). evidence (as shown in online suppl. Table S3). The NMA
For the VO2peak outcome, we analyzed 22 studies with results were similar to the pairwise meta-analysis. The
47 arms and seven types of interventions. The pairwise SUCRA ranking indicated that ICE was the most effective
meta-analysis results showed that, compared to UC, four form of exercise for improving Kt/V, followed by IAE. The
types of exercise (i.e., AE and combined aerobic and effect sizes paired with UC were 0.17 (0.06–0.28) and 0.13
resistance, both conducted during and outside of dialysis) (0.07–0.19), respectively (as shown in Table 2; online suppl.
significantly improved VO2peak with very low quality of Table S8; online suppl. Fig. S3). The confidence of the
the evidence (as shown in online suppl. Table S3). The evidence for interventions was low for Kt/V (as shown in
NMA results indicated that these four exercise types Table 3; online suppl. Table S9).
could improve VO2peak in MHD patients compared with For the physical component summary (PCS) of
UC. The SUCRA ranking indicated that, NCE was the HRQOL, we analyzed 23 studies with 53 arms and 10
most effective form of exercise for improving VO2peak. types of interventions. The pairwise meta-analysis results
This was followed by non-IAE and ICE. The effect sizes showed that, compared to UC, IAE and ICE could sig-
paired with UC were 4.35 (2.25–6.44), 4.31 (1.62–7.00), nificantly improve the PCS with very low and moderate

4 Am J Nephrol Hu/Wu/Kwok/Ho/Chau/Lok/Choi
DOI: 10.1159/000532109
Table 1. Types of interventions and controls of included studies

Types Description Number of Number of


arms participants

Intervention
IAE IAE typically involves patients pedaling on a cycle ergometer during hemodialysis 33 555
sessions, which occur 2–3 times per week at low to moderate intensity. The average
exercise duration is approximately 30 min per session
IRE IRE mainly consists of leg or nonvascular access side limb exercises performed during 19 408
hemodialysis sessions. These exercises typically involve the use of ankle weights,
dumbbells, elastic resistance bands, or weight training machines, and are conducted
at low to moderate intensity, 2–3 times per week
ICE ICE involves performing both AE and RE protocols, as described above, during 22 494
hemodialysis sessions
NAE NAE primarily consists of 15–45-min walking or cycling sessions performed at home, 9 188

Downloaded from http://karger.com/ajn/article-pdf/doi/10.1159/000532109/3998785/000532109.pdf by guest on 20 November 2023


outside of hemodialysis sessions, occurring 3–4 times per week
NRE NRE involves resistance training using light weights, dumbbells, resistance bands, or 2 72
weight machines with low to moderate loads, performed outside of hemodialysis
sessions, 3 times per week
NCE NCE involves performing both NAE and NRE protocols, typically 3–7 times per week, 10 234
outside of hemodialysis sessions
IIMT IIMT involves using a breathing training device to strengthen inspiratory muscles 3 63
during hemodialysis sessions, typically performed 3 times per week
NIMT NIMT involves practicing inspiratory muscle exercises with or without a breathing 3 70
training device outside of hemodialysis sessions, typically performed 2–7 times per
week
CIMT Combined inspiratory muscle training involves using a breathing training device 1 14
with a load of 50–70% maximum inspiration pressure to strengthen inspiratory
muscles both during hemodialysis (3 times weekly) and on non-hemodialysis days
(3 times weekly)
INES INES involves using electrical stimulation on the bilateral femoral quadriceps 5 72
muscles during hemodialysis for a duration of 20–40 min
IAE IAE combined with non-intradialytic resistance training involves performing 3 85
+ NRE exercises using dumbbells or fitness apparatus outside of hemodialysis sessions. The
program includes both AE and resistance training
IRE IRE combined with VR involves following the same RE protocol during hemodialysis 2 27
+ VR as described above. Additionally, up to 30 min of non-immersive gaming is used as a
form of VR to improve the dialysis experience
IAE IAE combined with BFR involves performing cycling exercises during hemodialysis 1 18
+ BFR with inflatable bands around both proximal thighs to reduce arterial blood flow by
50% in the lower limbs
IAE IAE combined with FT involves performing full range of motion exercises with 1 16
+ FT additional weights guided by a kinesiologist, three times a week during
hemodialysis. The program includes both AE and FT
NCE NCE is added to BE in a program that spans 24 weeks. The program includes a 1 26
+ BE combination of aerobic and RE in the first and third sessions of each week, while the
second and fourth sessions focus on BEs. The BE program includes stance exercise,
transition exercise, gait exercise, and functional strength exercises that last 30 min
per session
Control
UC “UC” refers to the standard care that is typically given to patients during 69 1,516
hemodialysis sessions
SE An SE intervention might involve simple stretching or low-load exercises that do not 12 226
provide a significant cardiovascular or resistance training stimulus

AE, aerobic exercise; RE, resistance exercise; IMT, inspiratory muscle training, BE, balance exercise; FT, functional training; BFR, blood
flow restriction; VR, virtual reality; UC, usual care; SE, sham exercise; INES, intradialytic neuromuscular electrical stimulation; IIMT, in-
tradialytic inspiratory muscle training; NIMT, non-intradialytic inspiratory muscle training; CIMT, combined inspiratory muscle training
during hemodialysis and non-hemodialysis days; IAE, intradialytic aerobic exercise; IRE, intradialytic resistance exercise; ICE, intradialytic
combined aerobic and resistance exercise; NAE, non-intradialytic aerobic exercise; NRE, non-intradialytic resistance exercise; NCE, non-
intradialytic combined aerobic and resistance exercise.

Exercise in Hemodialysis Patients Am J Nephrol 5


DOI: 10.1159/000532109
quality of the evidence (as shown in online suppl. Table Discussion
S3). The NMA results were similar to the pairwise meta-
analysis. The SUCRA ranking indicated that, IAE was the Summary of Study Findings
most effective form of exercise for improving PCS, fol- In this NMA of exercise in MHD patients, we found
lowed by ICE. The effect sizes paired with UC were 4.93 that the most effective interventions varied depending on
(2.31–7.54) and 3.90 (1.79–6.02), respectively (as shown the outcome of interest. IAE combined with BFR was the
in Table 2, online suppl. Table S10; online suppl. Fig. S4). most effective for the 6MWT; NCE was the most effective
The confidence of the evidence for interventions was for VO2peak; ICE was the most effective for Kt/V; IAE was
moderate for PCS (as shown in Table 3; online suppl. the most effective for the PCS of HRQOL; and NCE was
Table S11). the most effective for the MCS of HRQOL.
For the mental component summary (MCS) of ICE could improve all the above outcomes compared
HRQOL, 21 studies with 49 arms and 10 types of in- to the UC. Therefore, we first recommend this integrated
terventions were analyzed. The results from pairwise type of exercise for most MHD patients, especially those

Downloaded from http://karger.com/ajn/article-pdf/doi/10.1159/000532109/3998785/000532109.pdf by guest on 20 November 2023


meta-analysis showed that, compared to UC, IRE and who have the necessary exercise resources (e.g., equip-
intradialytic neuromuscular electrical stimulation could ment, knowledge, skills, and accessible exercise profes-
significantly improve the MCS with very low and low- sionals). In addition, IAE is also recommended (for those
quality evidence, respectively (as shown in online suppl. who have limited exercise resources) because this type of
Table S3). However, the results from NMA showed that exercise could benefit most outcomes (except MCS) and
IRE, ICE, and NCE could improve MCS for MHD pa- is easier to undertake than ICE. Exercise may have a
tients compared with UC. In addition, the SUCRA better effect on walking capacity if it is combined with
ranking indicated that NCE was the most effective form new elements, such as BFR or VR. Because the effect of
of exercise for improving MCS, followed by non-IAE. The exercise interventions on mental health is uncertain,
effect sizes paired with UC were 6.36 (0.45–12.27) and more attention needs to be paid to interventions that
8.19 (−5.98-22.37), respectively (as shown in Table 2; could improve MHD patients’ mental well-being.
online suppl. Table S12, and online suppl. Fig. S5). The
inconsistent results among pairwise meta-analysis, NMA, Interpretation
and SUCRA would downgrade the qualities of evidence. Out of the fifteen exercise modalities analyzed in this
The confidence of the evidence for interventions was low study, nine showed improvements in the 6MWT for
for MCS (as shown in Table 3; online suppl. Table S13). patients undergoing MHD. The improvement ranged
There was no evidence of publication bias for 6MWT (p = from 22.91 m (for IRE) to 97.35 m (for IAE combined
0.10), VO2peak (p = 0.66), Kt/V (p = 0.36), PCS (p = 0.63), with BFR) compared to the standard care for MHD
and MCS (p = 0.11) by Egger test and the NMA funnel patients. Given that the minimal clinically important
plot (as shown in online suppl. Fig. 6–10). difference for the 6MWT in similar patients is between
14.0 and 30.5 m [37, 38], we estimated the effect size to be
Exploration of Inconsistency moderate to large, with a moderate level of confidence in
The results from the global inconsistency test were not the evidence. The findings partially align with a published
significant (χ2 = 7.13, p = 0.99 for 6MWT; χ2 = 4.79, p = 0.57 Cochrane meta-analysis [39], which indicated that the
for VO2peak; χ2 = 6.74, p = 0.82 for Kt/V; χ2 = 13.56, p = 0.26 pooled effect of all exercise types on the 6MWT was an
for PCS; χ2 = 8.30, p = 0.69 for MCS). The local incon- improvement of 49.91 m for the same population.
sistency test using the side-splitting method showed that all However, our NMA offers additional insights by ranking
p values were larger than 0.05, indicating that the direct and different exercise types [13, 28, 39], showing that IAE
indirect comparisons between the two interventions were combined with BFR is likely the most effective inter-
consistent via the network and that NMA could be per- vention for improving the 6MWT. BFR exercise has been
formed for all outcomes by consistency models. reported as an effective complementary intervention for
deconditioned patients, as they can benefit from it even at
Risk of Bias across Studies low-intensity levels [7, 40]. Evidence suggests that low- to
The risk of bias assessment for included studies was moderate-intensity AE with BFR can improve body
presented in online supplementary Table S14. The overall composition and strength in both healthy individuals [41]
rates indicated that most of the studies have some con- and patients with chronic kidney diseases [7]. Although
cerns regarding the risk of bias, 76% for 6MWT, 64% for the published study showed that BFR exercises were safe
VO2peak, 70% for Kt/V, and 92% for HRQOL. in MHD patients, such techniques are complex and

6 Am J Nephrol Hu/Wu/Kwok/Ho/Chau/Lok/Choi
DOI: 10.1159/000532109
Downloaded from http://karger.com/ajn/article-pdf/doi/10.1159/000532109/3998785/000532109.pdf by guest on 20 November 2023

2
(For legend see next page.)

7
DOI: 10.1159/000532109
d

Am J Nephrol
Exercise in Hemodialysis Patients
b
a

c
should be conducted under the supervision of trained MCS score of HRQOL with pooled MDs of 3.65, 2.92, and
professionals [42, 43]. In addition, as only one study in 6.36 in MHD patients, respectively. Given that the minimal
our NMA examined this type of exercise, we must in- clinically important difference for the SF-36 scales is be-
terpret the results cautiously and encourage further re- tween three and five points [47, 48], we consider the effect
search on MHD patients. size for PCS to be small (with moderate confidence in the
Four types of exercise can enhance VO2peak in patients evidence) and the effect for MCS to be small to moderate
undergoing MHD, with improvements ranging from (with low confidence in the evidence). These results are
2.60 mL/kg per min (IAE) to 4.35 mL/kg per min (NCE) partially consistent with the published pairwise meta-
compared to UC. The minimal clinically important dif- analysis [18], which indicated that IAE, IRE, and ICE
ference for the VO2peak is 1.5 mL/kg per min for patients could improve PCS, while only IRE could improve MCS.
with chronic kidney diseases [44], and we estimated the We have greater confidence that IAE and ICE can enhance
effect size to be large although the evidence confidence is PCS, as supported by this NMA and similar published
low. This result is partly consistent with the published studies [11, 18, 28, 39, 49, 50]. Although NCE ranks first in

Downloaded from http://karger.com/ajn/article-pdf/doi/10.1159/000532109/3998785/000532109.pdf by guest on 20 November 2023


NMA, which indicated that CE is the most effective mo- improving MCS, we should interpret these results cau-
dality for enhancing VO2peak [12]. Our NMA showed that tiously due to the inconsistency of effects between the
NCE is a more effective exercise modality for improving pairwise meta-analysis and NMA, as well as the limited
VO2peak than other types of exercise. This superiority may number of NCE studies included in the MCS analysis.
be attributed to non-dialysis exercises potentially having a Therefore, more rigorous evidence is needed to determine
higher exercise intensity than intradialytic exercise, leading the improvement of MCS for MHD patients [5].
to greater cardiopulmonary benefits [23]. In this study, IAE is the most commonly reported
Compared to UC, IAE and ICE can improve Kt/V by exercise type, followed by ICE and IRE. This is consistent
0.13 and 0.17 in MHD patients, respectively. However, the with a published study that indicated intradialytic exercise
published meta-analysis did not find improvements in Kt/V as the most frequently reported type of exercise [23]. The
for IAE [11, 12] or all types of exercise [12, 39]. This proposed benefits of intradialytic exercise include time
discrepancy may arise from different classifications of ex- efficiency, ease of monitoring, low patient burden, and
ercise types and the larger number of studies included in our safety (as it is monitored by dialysis staff) [23]. Considering
NMA. Since Kt/V is calculated from the parameter during the barriers to exercise for MHD patients, such as low
the hemodialysis session [45], interventions conducted physical function, limited time, and limited exercise skills
during hemodialysis may have a better effect on improving and resources, intradialytic exercise is more suitable for
Kt/V compared to those conducted outside of hemodialysis. this population [23, 51]. IAE, which primarily involves
Exercise performed during hemodialysis can alter the he- pedaling a cycle ergometer during dialysis, is easier to
modynamics of MHD patients, allowing more fluids to perform than RE (i.e., several sets of resistance movements
reach the dialyzer, and subsequently improve Kt/V [8]. using different devices and workloads, requiring more
However, our NMA showed that IRE could not improve Kt/ exercise skills) [23]. Based on the results of this NMA, we
V, which is in line with published studies [12, 28, 39]. The recommend ICE and IAE for MHD patients who have
insignificant effect of IRE may be due to the limited number access to exercise resources, as these are more beneficial
of muscle groups that can move when resistance exercise is and easier to perform. These two types of exercises pos-
conducted during hemodialysis [23]. As a result, they may itively impact physical function (e.g., walking capacity,
not reach the “muscle morphologic threshold” necessary to cardiorespiratory fitness, and PCS) and dialysis adequacy.
increase muscle blood flow and remove urea toxins [46]. Additionally, further research exploring new elements that
The NMA results showed that IAE and ICE could could be combined with exercise, such as BFR and VR, is
improve the PCS score of HRQOL with pooled MDs of 4.93 warranted, as these elements may prove to be more ef-
and 3.90, respectively. IRE, ICE, and NCE can enhance the fective than exercise alone [23, 39].

Fig. 2. Network plots of studies examining the efficacy of exercise in intradialytic combined aerobic and resistance exercise; IIMT, intra-
MHD patients: a 6-min walking test; b peak oxygen uptake; c dialysis dialytic inspiratory muscle training; NIMT, non-intradialytic inspi-
adequacy; d physical component summary of HRQOL; e mental ratory muscle training; CIMT, combined inspiratory muscle training
component summary of HRQOL. IAE, intradialytic aerobic exercise; during hemodialysis and non-hemodialysis day; INES, intradialytic
IRE, intradialytic resistance exercise; ICE, intradialytic combined neuromuscular electrical stimulation; BE, balance exercise; FT,
aerobic and resistance exercise; NAE, non-intradialytic aerobic ex- functional training; BFR, blood flow restriction; VR, virtual reality;
ercise; NRE, non-intradialytic resistance exercise; NCE, non- UC, usual care; SE, sham exercise.

8 Am J Nephrol Hu/Wu/Kwok/Ho/Chau/Lok/Choi
DOI: 10.1159/000532109
Table 2. Network meta-analysis results

Intervention Comparison to UC, p value Probability of being best, % SUCRA, % Studies,* n Certainty
pooled MD (95% CI)

Six-minute walking test


SE −4.20 (−33.90, 25.50) 0.781 0 10.9 0 Very low
IAE 51.14 (28.21, 74.08) <0.001 0.2 63.7 9 Low
IRE 22.91 (1.63, 44.20) 0.035 0 33.6 5 Low
ICE 53.71 (30.08, 77.35) <0.001 0.4 66.4 6 Low
NAE 44.43 (21.45, 67.41) <0.001 0.2 56.0 5 Low
NCE 45.93 (12.03, 79.83) 0.008 0.2 56.9 2 Low
INES 25.27 (−17.11, 67.65) 0.243 0.1 37.1 3 Low
IIMT 77.27 (38.14, 116.40) <0.001 14.0 84.0 2 Very low
NIMT 11.77 (−34.94, 58.48) 0.621 0 26.0 1 Very low
CIMT −4.70 (−99.16, 89.76) 0.922 1.1 21.7 1 Low
IAE + BFR 97.35 (11.89, 182.81) 0.026 47.4 86.2 1 Low
IAE + NRE 28.49 (−37.56, 94.55) 0.398 1.3 41.8 0 Very low

Downloaded from http://karger.com/ajn/article-pdf/doi/10.1159/000532109/3998785/000532109.pdf by guest on 20 November 2023


IRE + VR 77.98 (5.85, 150.12) 0.034 23.9 78.8 1 Low
NCE + balance training 66.12 (7.88, 124.35) 0.026 11.1 73.9 0 Low
Peak oxygen uptake
IAE 2.60 (0.62, 4.57) 0.010 1.6 43.6 7 Very low
ICE 3.86 (2.24, 5.49) <0.001 12.2 68.1 7 Low
NAE 4.31 (1.62, 7.00) 0.002 32.4 75.1 3 Very low
NCE 4.35 (2.25, 6.44) <0.001 29.7 77.3 4 Low
INES 1.58 (−3.38, 6.54) 0.532 8.3 33.4 1 Very low
IAE + NRE 2.46 (−2.80, 7.72) 0.360 15.9 45.3 1 Very low
Dialysis adequacy
SE −0.07 (−0.25, 0.10) 0.410 0.1 20.1 0 Low
IAE 0.13 (0.07, 0.19) <0.001 9.2 79.2 14 Low
IRE 0.07 (−0.02, 0.15) 0.116 1.1 59.4 8 Low
ICE 0.17 (0.06, 0.28) 0.002 32.1 88.0 3 Low
NRE −0.13 (−0.32, 0.05) 0.155 0.1 9.8 2 Very low
NCE 0.14 (−0.10, 0.38) 0.248 30.7 74.6 0 Low
IIMT 0.04 (−0.20, 0.28) 0.719 10.5 50.7 1 Very low
INES −0.03 (−0.19, 0.14) 0.746 0.6 31.3 2 Very low
IAE + NRE 0.02 (−0.14, 0.18) 0.840 2.0 43.0 2 Very low
IAE + FT 0.07 (−0.16, 0.31) 0.549 13.6 57.8 0 Very low
Physical component summary of HRQOL
SE 1.06 (−4.00, 6.12) 0.682 1.3 38.3 0 Very low
IAE 4.93 (2.31, 7.54) <0.001 32.5 85.4 6 Moderate
IRE 3.06 (−0.43, 6.55) 0.086 6.7 61.7 3 Low
ICE 3.90 (1.79, 6.02) <0.001 9.1 73.0 7 Very low
NAE 2.58 (−3.64, 8.79) 0.416 14.4 54.8 1 Low
NCE 1.62 (−3.66, 6.90) 0.547 6.1 45.4 0 Very low
IIMT 1.79 (−5.34, 8.92) 0.623 13.3 48.6 0 Very low
NIMT −5.44 (−10.83, −0.05) 0.048 0 2.1 1 Low
INES 3.54 (−0.80, 7.88) 0.110 16.7 66.1 2 Low
Mental component summary of HRQOL
SE 4.78 (−0.42, 9.98) 0.071 4.4 62.5 0 Low
IAE 0.33 (−2.51, 3.16) 0.820 0 15.9 6 Moderate
IRE 3.65 (0.07, 7.24) 0.046 0.7 52.0 3 Moderate
ICE 2.92 (0.12, 5.72) 0.041 0 44.2 6 Moderate
NAE 8.19 (−5.98, 22.37) 0.257 39.8 72.1 1 Very low
NCE 6.36 (0.45, 12.27) 0.035 16.0 74.5 0 Moderate
IIMT 3.97 (−17.67, 25.62) 0.719 27.8 50.5 0 Very low
NIMT 5.31 (−0.52, 11.14) 0.074 10.1 65.5 1 Low
INES 3.51 (−0.22, 7.24) 0.065 1.3 51.1 2 Moderate

Numbers in bold represent statistically significant results. MD, mean difference; 95% CI, 95% confidence interval; AE, aerobic exercise; RE, resistance
exercise; CE, combined aerobic and resistance exercise; IIMT, intradialytic inspiratory muscle training; CIMT, combined inspiratory muscle training during
hemodialysis and non-hemodialysis day; INES, intradialytic neuromuscular electrical stimulation; SUCRA, surface under the cumulative ranking; FT,
functional training; BFR, blood flow restriction; VR, virtual reality; UC, usual care; SE, sham exercise; NIMT, non-intradialytic inspiratory muscle training; IAE,
intradialytic aerobic exercise; IRE, intradialytic resistance exercise; ICE, intradialytic combined aerobic and resistance exercise; NAE, non-intradialytic aerobic
exercise; NRE, non-intradialytic resistance exercise; NCE, non-intradialytic combined aerobic and resistance exercise; HRQOL, health-related quality of life.
*Number of direct comparison studies.

Exercise in Hemodialysis Patients Am J Nephrol 9


DOI: 10.1159/000532109
Table 3. Summary of confidence in the ranking of treatments for outcomes (GRADE approach)

Outcomes Study limitations Indirectness Inconsistency Imprecision Publication Confidence


bias

Six-minute walking test Some concerns* No concerns No concerns No concerns No concerns Moderate
Peak oxygen uptake Some concerns* No concerns Some concernsa No concerns No concerns Low
Dialysis adequacy Some concerns* No concerns Some concernsa No concerns No concerns Low
Physical component summary Some concerns* No concerns No concerns No concerns No concerns Moderate
of HRQOL
Mental component summary of Some concerns* No concerns No concerns Some No concerns Low
HRQOL concernsb

GRADE, Grading of Recommendations Assessment, Development and Evaluation; HRQOL, health-related quality of life. *Evidence came
from >85% some concerns or high risk of bias studies (as shown in supplement Table S14). aHigh heterogeneity. bSome concerns of
imprecision.

Downloaded from http://karger.com/ajn/article-pdf/doi/10.1159/000532109/3998785/000532109.pdf by guest on 20 November 2023


This NMA has several strengths. Firstly, it focuses on into the impact of exercise on this population. Tailoring
the outcomes that are most relevant to MHD patients, exercise programs to individual patients’ conditions and
including physical fitness, clinical indicators, and available resources is also essential.
HRQOL. Secondly, the review employs a systematic
search strategy and rigorous analysis methodology.
Lastly, by including studies published in both English Statement of Ethics
and Chinese, the review captures a broader range of
research conducted on a larger population. An ethics statement is not applicable because this study is based
exclusively on published literature.
Limitations
Despite its strengths, there are some limitations that
cannot be overlooked. The methodology of the included Conflict of Interest Statement
studies was generally rated as moderate to high risk. Some
exercise types that ranked high in effect comparisons The authors declare that they have no conflicts of interest.
were based on only one or two studies, which could result
in less stable conclusions. Finally, this study focused
solely on the effects of different types of exercises, while Funding Sources
variations in frequency, duration, and intensity across the
included studies may have influenced the results. This study did not receive any funding support.

Author Contributions
Conclusions
Huagang Hu and Chanchan Wu: conceptualization, method-
In comparison to other forms of exercise, ICE may be the ology, software, formal analysis, writing-original draft,
most suitable option, as it significantly improves multiple writing – review and editing, and project administration. Jojo Yan
outcomes. MHD patients should be encouraged to engage Yan Kwok, Mu-Hsing Ho, and Kris Yuet Wan Lok: methodology,
and writing – review and editing. Pui Hing Chau: methodology,
in this type of exercise if they have access to the necessary validation, data curation and writing – review and editing. Ed-
resources. IAE is also recommended, as it has a notable mond Pui Hang Choi: conceptualization, methodology, data cu-
impact on most outcomes (except MCS) and is easier to ration, writing – review and editing, and supervision.
undertake than CE. Further research is warranted to explore
the effects of combined exercise with novel elements, such
as BFR and VR, as these may enhance the benefits beyond Data Availability Statement
traditional exercise alone. Additionally, studies investigating All data generated or analyzed during this study are included in
the effects of varying exercise duration, intensity, and fre- this article and in its supplementary materials. Further inquiries
quency are needed to provide more comprehensive insights can be directed to the corresponding author.

10 Am J Nephrol Hu/Wu/Kwok/Ho/Chau/Lok/Choi
DOI: 10.1159/000532109
References

1 Liyanage T, Ninomiya T, Jha V, Neal B, Patrice disease: systematic review and network meta- dialysis patients. Blood Purif. 2020;49(1–2):
HM, Okpechi I, et al. Worldwide access to analysis. J Physiother. 2019;65(1):4–15. 151–7.
treatment for end-stage kidney disease: a sys- 13 Ferrari F, Helal L, Dipp T, Soares D, Soldatelli 24 Higgins JPT, Thomas J, Chandler J, Cump-
tematic review. Lancet. 2015;385(9981):1975–82. Â, Mills AL, et al. Intradialytic training in ston M, Li T, Page MJ, et al. Cochrane
2 Eckert K, Motemaden L, Alves M. Effect of patients with end-stage renal disease: a sys- handbook for systematic reviews of inter-
hemodialysis compared with conservative tematic review and meta-analysis of ran- ventions. 2nd ed. Hoboken (NJ): Wiley-
management on quality of life in older adults domized clinical trials assessing the effects of Blackwell; 2019.
with end-stage renal disease: systematic re- five different training interventions. 25 Heiwe S, Jacobson SH. Exercise training for
view. J Hosp Palliat Nurs. 2018;20(3):279–85. J Nephrol. 2020;33(2):251–66. adults with chronic kidney disease. Co-
3 Evangelidis N, Tong A, Manns B, Hemmel- 14 Bundchen DC, Sousa H, Afreixo V, Frontini chrane Database Syst Rev. 2011;2011(10):
garn B, Wheeler DC, Tugwell P, et al. De- R, Ribeiro O, Figueiredo D, et al. Intradialytic CD003236.
veloping a set of core outcomes for trials in exercise in end-stage renal disease: an um- 26 Gomes Neto M, de Lacerda FFR, Lopes AA,
hemodialysis: an international Delphi survey. brella review of systematic reviews and/or Martinez BP, Saquetto MB. Intradialytic ex-
Am J Kidney Dis. 2017;70(4):464–75. meta-analytical studies. Clin Rehabil. 2021; ercise training modalities on physical func-
4 Jegatheesan DK, Modderman R, Krishnas- 35(6):812–28. tioning and health-related quality of life in

Downloaded from http://karger.com/ajn/article-pdf/doi/10.1159/000532109/3998785/000532109.pdf by guest on 20 November 2023


amy R, Tong A, Coombes JS, Viecelli AK, 15 Clyne N, Anding-Rost K. Exercise training in patients undergoing maintenance hemodial-
et al. A systematic review of scope and chronic kidney disease-effects, expectations ysis: systematic review and meta-analysis.
consistency of outcome measures for physical and adherence. Clin Kidney J. 2021;14(Suppl Clin Rehabil. 2018;32(9):1189–202.
fitness in chronic kidney disease trials. Kid- 2):ii3–ii14. 27 Young HML, March DS, Graham-Brown
ney Int Rep. 2021;6(5):1280–8. 16 Deligiannis A, D’Alessandro C, Cupisti A. MPM, Jones AW, Curtis F, Grantham CS,
5 Mapes DL, Lopes AA, Satayathum S, Mccul- Exercise training in dialysis patients: impact et al. Effects of intradialytic cycling exercise
lough KP, Goodkin DA, Locatelli F, et al. on cardiovascular and skeletal muscle health. on exercise capacity, quality of life, physical
Health-related quality of life as a predictor of Clin Kidney J. 2021;14(Suppl 2):ii25–ii33. function and cardiovascular measures in
mortality and hospitalization: the Dialysis 17 Zhang F, Zhou WQ, Sun QZ, Zhai YY, Zhang adult haemodialysis patients: a systematic
Outcomes and Practice Patterns Study Y, Su H, et al. Effects of intradialytic resis- review and meta-analysis. Nephrol Dial
(DOPPS). Kidney Int. 2003;64(1):339–49. tance exercises on physical performance, Transplant. 2018;33(8):1436–45.
6 Ashby D, Borman N, Burton J, Corbett R, nutrient intake and quality of life among 28 Huang M, Lv AL, Wang J, Xu N, Ma GR, Zhai
Davenport A, Farrington K, et al. Renal haemodialysis people: a systematic review ZH, et al. Exercise training and outcomes in
association clinical practice guideline on and meta-analysis. Nurs Open. 2021;8(2): hemodialysis patients: systematic review and
haemodialysis. BMC Nephrol. 2019; 529–38. meta-analysis. Am J Nephrol. 2019;50(4):
20(1):379. 18 Hu H, Liu X, Chau PH, Choi EPH. Effects of 240–54.
7 Wilkinson TJ, McAdams-DeMarco M, Ben- intradialytic exercise on health-related qual- 29 Ware JE. SF-36 health survey update. Spine.
nett PN, Wilund K; Global Renal Exercise ity of life in patients undergoing maintenance 2000;25(24):3130–9.
Network. Advances in exercise therapy in haemodialysis: a systematic review and meta- 30 Sterne JAC, Savović J, Page MJ, Elbers RG,
predialysis chronic kidney disease, hemodi- analysis. Qual Life Res. 2022;31(7):1915–32. Blencowe NS, Boutron I, et al. RoB 2: a re-
alysis, peritoneal dialysis, and kidney trans- 19 Dias EC, Orcy R, Antunes MF, Kohn R, vised tool for assessing risk of bias in rand-
plantation. Curr Opin Nephrol Hypertens. Rombaldi AJ, Ribeiro L, et al. Intradialytic omised trials. BMJ. 2019;366:l4898.
2020;29(5):471–9. exercise with blood flow restriction: some- 31 Salanti G, Del Giovane C, Chaimani A,
8 Ferreira GD, Bohlke M, Correa CM, Dias EC, thing to add to hemodialysis adequacy? Caldwell DM, Higgins JP. Evaluating the
Orcy RB. Does intradialytic exercise improve Findings from a crossover study. Hemodial quality of evidence from a network meta-
removal of solutes by hemodialysis? A sys- Int. 2020;24(1):71–8. analysis. PLoS One. 2014;9(7):e99682.
tematic review and meta-analysis. Arch Phys 20 Hutton B, Salanti G, Caldwell DM, Chaimani 32 Nikolakopoulou A, Higgins JPT, Papakon-
Med Rehabil. 2019;100(12):2371–80. A, Schmid CH, Cameron C, et al. The stantinou T, Chaimani A, Del Giovane C,
9 Kirkman DL, Scott M, Kidd J, Macdonald JH. PRISMA extension statement for reporting of Egger M, et al. CINeMA: an approach for
The effects of intradialytic exercise on he- systematic reviews incorporating network assessing confidence in the results of a net-
modialysis adequacy: a systematic review. meta-analyses of health care interventions: work meta-analysis. PLoS Med. 2020;17(4):
Semin Dial. 2019;32(4):368–78. checklist and explanations. Ann Intern Med. e1003082.
10 Pu J, Jiang Z, Wu WH, Li L, Zhang LL, Li Y, 2015;162(11):777–84. 33 Borenstein M, Hedges LV, Higgins JP, Roth-
et al. Efficacy and safety of intradialytic ex- 21 Song Y, Chen L, Wang M, He Q, Xue J, Jiang stein HR. A basic introduction to fixed-effect
ercise in haemodialysis patients: a systematic H. The optimal exercise modality and in- and random-effects models for meta-analysis.
review and meta-analysis. BMJ Open. 2019; tensity for hemodialysis patients incorpo- Res Synth Methods. 2010;1(2):97–111.
9(1):e020633. rating Bayesian network meta-analysis and 34 Higgins JP, Thompson SG. Quantifying
11 Salhab N, Karavetian M, Kooman J, Fiacca- systematic review. Front Physiol. 2022;13: heterogeneity in a meta-analysis. Stat Med.
dori E, El Khoury CF. Effects of intradialytic 945465. 2002;21(11):1539–58.
aerobic exercise on hemodialysis patients: a 22 Zang W, Fang M, He H, Mu L, Zheng X, Shu 35 Shim S, Yoon BH, Shin IS, Bae JM. Network
systematic review and meta-analysis. H, et al. Comparative efficacy of exercise meta-analysis: application and practice us-
J Nephrol. 2019;32(4):549–66. modalities for cardiopulmonary function in ing Stata. Epidemiol Health. 2017;39:
12 Scapini KB, Bohlke M, Moraes OA, Ro- hemodialysis patients: a systematic review e2017047.
drigues CG, Inacio JFS, Sbruzzi G, et al. and network meta-analysis. Front Public 36 Mbuagbaw L, Rochwerg B, Jaeschke R, Heels-
Combined training is the most effective Health. 2022;10:1040704. Andsell D, Alhazzani W, Thabane L, et al.
training modality to improve aerobic capacity 23 Fang HY, Burrows BT, King AC, Wilund KR. Approaches to interpreting and choosing the
and blood pressure control in people re- A comparison of intradialytic versus out-of- best treatments in network meta-analyses.
quiring haemodialysis for end-stage renal clinic exercise training programs for hemo- Syst Rev. 2017;6(1):79.

Exercise in Hemodialysis Patients Am J Nephrol 11


DOI: 10.1159/000532109
37 Segura-Ortí E, Martínez-Olmos FJ. Test- 42 Rolnick N, Kimbrell K, Cerqueira MS, 47 Stewart AL, Greenfield S, Hays RD, Wells K,
retest reliability and minimal detectable Weatherford B, Brandner C. Perceived bar- Rogers WH, Berry SD. Functional status and
change scores for sit-to-stand-to-sit tests, the riers to blood flow restriction training. Front well-being of patients with chronic condi-
six-minute walk test, the one-leg heel-rise Rehabil Sci. 2021;2(2):1–8. tions. Results from the Medical Outcomes
test, and handgrip strength in people un- 43 Rolnick N, de Sousa Neto IV, da Fonseca EF, Study. JAMA. 1989;262(7):907–13.
dergoing hemodialysis. Phys Ther. 2011; Neves RVP, Rosa TDS, Nascimento DDC. 48 Strand V, Boers M, Idzerda L, Kirwan JR,
91(8):1244–52. Potential implications of blood flow restric- Kvien TK, Tugwell PS, et al. It’s good to feel
38 Bohannon RW, Crouch R. Minimal clinically tion exercise on patients with chronic kidney better but it’s better to feel good and even
important difference for change in 6-minute disease: a brief review. J Exerc Rehabil. 2022; better to feel good as soon as possible for as
walk test distance of adults with pathology: a 18(2):81–95. long as possible. Response criteria and the
systematic review. J Eval Clin Pract. 2017; 44 Wilkinson TJ, Watson EL, Xenophontos S, importance of change at OMERACT 10.
23(2):377–81. Gould DW, Smith AC. The “Minimum Clini- J Rheumatol. 2011;38(8):1720–7.
39 Bernier-Jean A, Beruni NA, Bondonno NP, cally Important Difference” in frequently re- 49 Sheng KX, Zhang P, Chen LL, Cheng J, Wu CC,
Williams G, Teixeira-Pinto A, Craig JC, et al. ported objective physical function tests after a Chen JH. Intradialytic exercise in hemodialysis
Exercise training for adults undergoing 12-Week renal rehabilitation exercise inter- patients: a systematic review and meta-analysis.
maintenance dialysis. Cochrane Database vention in nondialysis chronic kidney disease. Am J Nephrol. 2014;40(5):478–90.
Syst Rev. 2022;1:CD014653. Am J Phys Med Rehabil. 2019;98(6):431–7. 50 Chung YC, Yeh ML, Liu YM. Effects of intra-

Downloaded from http://karger.com/ajn/article-pdf/doi/10.1159/000532109/3998785/000532109.pdf by guest on 20 November 2023


40 Kirkman DL, Bohmke N, Carbone S, Garten 45 National Kidney Foundation. KDOQI clini- dialytic exercise on the physical function, de-
RS, Rodriguez-Miguelez P, Franco RL, et al. cal practice guideline for hemodialysis ade- pression and quality of life for haemodialysis
Exercise intolerance in kidney diseases: quacy: 2015 update. Am J Kidney Dis. 2015; patients: a systematic review and meta-analysis
physiological contributors and therapeutic 66(5):884–930. of randomised controlled trials. J Clin Nurs.
strategies. Am J Physiol Renal Physiol. 2021; 46 Pellizzaro CO, Thomé FS, Veronese FV. Ef- 2017;26(13–14):1801–13.
320(2):F161–73. fect of peripheral and respiratory muscle 51 Li T, Lv A, Xu N, Huang M, Su Y, Zhang B, et al.
41 Pope ZK, Willardson JM, Schoenfeld BJ. training on the functional capacity of he- Barriers and facilitators to exercise in haemo-
Exercise and blood flow restriction. J Strength modialysis patients. Ren Fail. 2013;35(2): dialysis patients: a systematic review of quali-
Cond Res. 2013;27(10):2914–26. 189–97. tative studies. J Adv Nurs. 2021;77(12):4679–92.

12 Am J Nephrol Hu/Wu/Kwok/Ho/Chau/Lok/Choi
DOI: 10.1159/000532109

You might also like